Glia-derived ATP inversely regulates excitability of pyramidal and CCK-positive neurons

Zhibing Tan, Yu Liu, Wang Xi, Hui Fang Lou, Liya Zhu, Zhifei Guo, Lin Mei, Shumin Duan

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

Astrocyte responds to neuronal activity with calcium waves and modulates synaptic transmission through the release of gliotransmitters. However, little is known about the direct effect of gliotransmitters on the excitability of neuronal networks beyond synapses. Here we show that selective stimulation of astrocytes expressing channelrhodopsin-2 in the CA1 area specifically increases the firing frequency of CCK-positive but not parvalbumin-positive interneurons and decreases the firing rate of pyramidal neurons, phenomena mimicked by exogenously applied ATP. Further evidences indicate that ATP-induced increase and decrease of excitability are caused, respectively, by P2Y1 receptor-mediated inhibition of a two-pore domain potassium channel and A1 receptor-mediated opening of a G-protein-coupled inwardly rectifying potassium channel. Moreover, the activation of ChR2-expressing astrocytes reduces the power of kainate-induced hippocampal ex vivo gamma oscillation. Thus, through distinct receptor subtypes coupled with different K+ channels, astrocyte-derived ATP differentially modulates the excitability of different types of neurons and efficiently controls the activity of neuronal network.

Original languageEnglish (US)
Article number13772
JournalNature Communications
Volume8
DOIs
StatePublished - Jan 27 2017

Fingerprint

adenosine triphosphate
neurons
Neuroglia
Astrocytes
Neurons
Adenosine Triphosphate
synapses
G Protein-Coupled Inwardly-Rectifying Potassium Channels
Purinergic P2Y1 Receptors
stimulation
Parvalbumins
Calcium Signaling
Pyramidal Cells
calcium
Kainic Acid
Potassium Channels
Interneurons
Synaptic Transmission
activation
Synapses

ASJC Scopus subject areas

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

Cite this

Glia-derived ATP inversely regulates excitability of pyramidal and CCK-positive neurons. / Tan, Zhibing; Liu, Yu; Xi, Wang; Lou, Hui Fang; Zhu, Liya; Guo, Zhifei; Mei, Lin; Duan, Shumin.

In: Nature Communications, Vol. 8, 13772, 27.01.2017.

Research output: Contribution to journalArticle

Tan, Zhibing ; Liu, Yu ; Xi, Wang ; Lou, Hui Fang ; Zhu, Liya ; Guo, Zhifei ; Mei, Lin ; Duan, Shumin. / Glia-derived ATP inversely regulates excitability of pyramidal and CCK-positive neurons. In: Nature Communications. 2017 ; Vol. 8.
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AU - Guo, Zhifei

AU - Mei, Lin

AU - Duan, Shumin

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